Determining whether seed production is pollen limited has been an area of intensive empirical study over the last two decades. Yet current evidence does not allow satisfactory assessment of the causes or consequences of pollen limitation. Here, we critically evaluate existing theory and issues concerning pollen limitation. Our main conclusion is that a change in approach is needed to determine whether pollen limitation reflects random fluctuations around a pollen-resource equilibrium, an adaptation to stochastic pollination environments, or a chronic syndrome caused by an environmental perturbation. We formalize and extend D. Haig and M. Westoby's conceptual model, and illustrate its use in guiding research on the evolutionary consequences of pollen limitation, i.e., whether plants evolve or have evolved to ameliorate pollen limitation. This synthesis also reveals that we are only beginning to understand when and how pollen limitation at the plant level translates into effects on plant population dynamics. We highlight the need for both theoretical and empirical approaches to gain a deeper understanding of the importance of life-history characters, Allee effects, and environmental perturbations in population declines mediated by pollen limitation. Lastly, our synthesis identifies a critical need for research on potential effects of pollen limitation at the community and ecosystem levels.
Quantifying the extent to which seed production is limited by the availability of pollen has been an area of intensive empirical study over the past few decades. Whereas theory predicts that pollen augmentation should not increase seed production, numerous empirical studies report significant and strong pollen limitation. Here, we use a variety of approaches to examine the correlates of pollen limitation in an effort to understand its occurrence and importance in plant evolutionary ecology. In particular, we examine the role of recent ecological perturbations in influencing pollen limitation and discuss the relation between pollen limitation and plant traits. We find that the magnitude of pollen limitation observed in natural populations depends on both historical constraints and contemporary ecological factors.
Using historic data sets, we quantified the degree to which global change over 120 years disrupted plant-pollinator interactions in a temperate forest understory community in Illinois, USA. We found degradation of interaction network structure and function and extirpation of 50% of bee species. Network changes can be attributed to shifts in forb and bee phenologies resulting in temporal mismatches, nonrandom species extinctions, and loss of spatial co-occurrences between extant species in modified landscapes. Quantity and quality of pollination services have declined through time. The historic network showed flexibility in response to disturbance; however, our data suggest that networks will be less resilient to future changes.
Abstract. Both means and year-to-year variances of climate variables such as temperature and precipitation are predicted to change. However, the potential impact of changing climatic variability on the fate of populations has been largely unexamined. We analyzed multiyear demographic data for 36 plant and animal species with a broad range of life histories and types of environment to ask how sensitive their long-term stochastic population growth rates are likely to be to changes in the means and standard deviations of vital rates (survival, reproduction, growth) in response to changing climate. We quantified responsiveness using elasticities of the long-term population growth rate predicted by stochastic projection matrix models. Short-lived species (insects and annual plants and algae) are predicted to be more strongly (and negatively) affected by increasing vital rate variability relative to longer-lived species (perennial plants, birds, ungulates). Taxonomic affiliation has little power to explain sensitivity to increasing variability once longevity has been taken into account. Our results highlight the potential vulnerability of short-lived species to an increasingly variable climate, but also suggest that problems associated with short-lived undesirable species (agricultural pests, disease vectors, invasive weedy plants) may be exacerbated in regions where climate variability decreases.
Predation can be intense, creating strong direct and indirect effects throughout food webs. In addition, ecologists increasingly recognize that fluxes of organisms across ecosystem boundaries can have major consequences for community dynamics. Species with complex life histories often shift habitats during their life cycles and provide potent conduits coupling ecosystems. Thus, local interactions that affect predator abundance in one ecosystem (for example a larval habitat) may have reverberating effects in another (for example an adult habitat). Here we show that fish indirectly facilitate terrestrial plant reproduction through cascading trophic interactions across ecosystem boundaries. Fish reduce larval dragonfly abundances in ponds, leading to fewer adult dragonflies nearby. Adult dragonflies consume insect pollinators and alter their foraging behaviour. As a result, plants near ponds with fish receive more pollinator visits and are less pollen limited than plants near fish-free ponds. Our results confirm that strong species interactions can reverberate across ecosystems, and emphasize the importance of landscape-level processes in driving local species interactions.
There is little consensus about how natural (e.g. productivity, disturbance) and anthropogenic (e.g. invasive species, habitat destruction) ecological drivers influence biodiversity. Here, we show that when sampling is standardised by area (species density) or individuals (rarefied species richness), the measured effect sizes depend critically on the spatial grain and extent of sampling, as well as the size of the species pool. This compromises comparisons of effects sizes within studies using standard statistics, as well as among studies using meta-analysis. To derive an unambiguous effect size, we advocate that comparisons need to be made on a scale-independent metric, such as Hurlbert's Probability of Interspecific Encounter. Analyses of this metric can be used to disentangle the relative influence of changes in the absolute and relative abundances of individuals, as well as their intraspecific aggregations, in driving differences in biodiversity among communities. This and related approaches are necessary to achieve generality in understanding how biodiversity responds to ecological drivers and will necessitate a change in the way many ecologists collect and analyse their data.
Although invasive plant species often reduce diversity, they rarely cause plant extinctions. We surveyed paired invaded and uninvaded plant communities from three biomes. We reconcile the discrepancy in diversity loss from invaders by showing that invaded communities have lower local richness but steeper species accumulation with area than that of uninvaded communities, leading to proportionately fewer species loss at broader spatial scales. We show that invaders drive scale-dependent biodiversity loss through strong neutral sampling effects on the number of individuals in a community. We also show that nonneutral species extirpations are due to a proportionately larger effect of invaders on common species, suggesting that rare species are buffered against extinction. Our study provides a synthetic perspective on the threat of invasions to biodiversity loss across spatial scales.
Our understanding of pollen limitation depends on a realistic view of its magnitude. Previous reviews of pollen supplementation experiments concluded that a majority of plant species suffers from pollen limitation and that its magnitude is high. Here, we perform a meta-analysis and find evidence that publication bias, experimental design, and the response variable chosen all influence the magnitude of pollen limitation. Fail-safe numbers indicate that publication bias exists for some measures of pollen limitation; significant results are more likely to be published and therefore available for review. Moreover, experiments conducted on only a fraction of a plant's flowers and reproductive episodes report ~8-fold higher effect sizes than those on all flowers produced over the entire lifetime, likely because resource reallocation among flowers and across years contributes to estimates of pollen limitation. Studies measuring percentage fruit set report higher values of pollen limitation than those measuring other response variables, such as seeds per fruit, perhaps because many plant species will not produce fruits unless adequate pollen receipt occurs to fertilize most ovules. We offer suggestions for reducing the bias introduced by methodology in pollen supplementation experiments and discuss our results in the context of optimality theory.
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